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Published in: Current Hepatology Reports 1/2017

01-03-2017 | Hepatic Cancer (A Singal and A Mufti, Section Editors)

Tailored Algorithms for Hepatocellular Carcinoma Surveillance: Is One-Size-Fits-All Strategy Outdated?

Authors: Nicolas Goossens, C. Billie Bian, Yujin Hoshida

Published in: Current Hepatology Reports | Issue 1/2017

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Abstract

Purpose of Review

Current clinical practice guidelines recommend regular hepatocellular carcinoma (HCC) surveillance with biannual ultrasound with or without serum alpha-fetoprotein uniformly applied to all patients with cirrhosis. However, clinical implementation of this one-size-fits-all strategy has been challenging as evidenced by very low application rate below 20% due to various reasons, including suboptimal performance of the surveillance modalities.

Recent Findings

Newly emerging imaging techniques such as abbreviated MRI (AMRI) and molecular HCC risk biomarkers have increasingly become available for clinical evaluation and implementation. These technologies may have a potential to reshape HCC surveillance by enabling tailored strategies. This would involve performing optimized surveillance tests according to individual HCC risk and allocating limited medical resources for HCC surveillance based on cost-effectiveness.

Summary

Tailored HCC surveillance could lead to achievement of precision HCC care and substantial improvement of the current dismal patient prognosis.
Literature
3.
go back to reference Harris RJ, Thomas B, Griffiths J, Costella A, Chapman R, Ramsay M, et al. Increased uptake and new therapies are needed to avert rising hepatitis C-related end stage liver disease in England: modelling the predicted impact of treatment under different scenarios. J Hepatol. 2014;61(3):530–7. doi:10.1016/j.jhep.2014.05.008.CrossRefPubMed Harris RJ, Thomas B, Griffiths J, Costella A, Chapman R, Ramsay M, et al. Increased uptake and new therapies are needed to avert rising hepatitis C-related end stage liver disease in England: modelling the predicted impact of treatment under different scenarios. J Hepatol. 2014;61(3):530–7. doi:10.​1016/​j.​jhep.​2014.​05.​008.CrossRefPubMed
4.
9.
go back to reference Kansagara D, Papak J, Pasha AS, O’Neil M, Freeman M, Relevo R, et al. Screening for hepatocellular carcinoma in chronic liver disease: a systematic review. Ann Intern Med. 2014;161(4):261–9. doi:10.7326/M14-0558.CrossRefPubMed Kansagara D, Papak J, Pasha AS, O’Neil M, Freeman M, Relevo R, et al. Screening for hepatocellular carcinoma in chronic liver disease: a systematic review. Ann Intern Med. 2014;161(4):261–9. doi:10.​7326/​M14-0558.CrossRefPubMed
10.
go back to reference Poustchi H, Farrell GC, Strasser SI, Lee AU, McCaughan GW, George J. Feasibility of conducting a randomized control trial for liver cancer screening: is a randomized controlled trial for liver cancer screening feasible or still needed? Hepatology. 2011;54(6):1998–2004.CrossRefPubMed Poustchi H, Farrell GC, Strasser SI, Lee AU, McCaughan GW, George J. Feasibility of conducting a randomized control trial for liver cancer screening: is a randomized controlled trial for liver cancer screening feasible or still needed? Hepatology. 2011;54(6):1998–2004.CrossRefPubMed
12.
go back to reference Singal AG, Nehra M, Adams-Huet B, Yopp AC, Tiro JA, Marrero JA, et al. Detection of hepatocellular carcinoma at advanced stages among patients in the HALT-C trial: where did surveillance fail? Am J Gastroenterol. 2013;108(3):425–32. doi:10.1038/ajg.2012.449.CrossRefPubMed Singal AG, Nehra M, Adams-Huet B, Yopp AC, Tiro JA, Marrero JA, et al. Detection of hepatocellular carcinoma at advanced stages among patients in the HALT-C trial: where did surveillance fail? Am J Gastroenterol. 2013;108(3):425–32. doi:10.​1038/​ajg.​2012.​449.CrossRefPubMed
13.
go back to reference Del Poggio P, Olmi S, Ciccarese F, Di Marco M, Rapaccini GL, Benvegnu L, et al. Factors that affect efficacy of ultrasound surveillance for early stage hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol. 2014;12(11):1927–33. doi:10.1016/j.cgh.2014.02.025. e2.CrossRefPubMed Del Poggio P, Olmi S, Ciccarese F, Di Marco M, Rapaccini GL, Benvegnu L, et al. Factors that affect efficacy of ultrasound surveillance for early stage hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol. 2014;12(11):1927–33. doi:10.​1016/​j.​cgh.​2014.​02.​025. e2.CrossRefPubMed
15.
go back to reference Mourad A, Deuffic-Burban S, Ganne-Carrie N, Renaut-Vantroys T, Rosa I, Bouvier AM, et al. Hepatocellular carcinoma screening in patients with compensated hepatitis C virus (HCV)-related cirrhosis aware of their HCV status improves survival: a modeling approach. Hepatology. 2014;59(4):1471–81. doi:10.1002/hep.26944.CrossRefPubMed Mourad A, Deuffic-Burban S, Ganne-Carrie N, Renaut-Vantroys T, Rosa I, Bouvier AM, et al. Hepatocellular carcinoma screening in patients with compensated hepatitis C virus (HCV)-related cirrhosis aware of their HCV status improves survival: a modeling approach. Hepatology. 2014;59(4):1471–81. doi:10.​1002/​hep.​26944.CrossRefPubMed
18.
go back to reference Gupta S, Bent S, Kohlwes J. Test characteristics of α-fetoprotein for detecting hepatocellular carcinoma in patients with hepatitis C: a systematic review and critical analysis. Ann Intern Med. 2003;139(1):46–50.CrossRefPubMed Gupta S, Bent S, Kohlwes J. Test characteristics of α-fetoprotein for detecting hepatocellular carcinoma in patients with hepatitis C: a systematic review and critical analysis. Ann Intern Med. 2003;139(1):46–50.CrossRefPubMed
19.
go back to reference Mancebo A, González–Diéguez ML, Cadahía V, Varela M, Pérez R, Navascués CA, et al. Annual incidence of hepatocellular carcinoma among patients with alcoholic cirrhosis and identification of risk groups. Clin Gastroenterol Hepatol. 2013;11(1):95–101. doi:10.1016/j.cgh.2012.09.007.CrossRefPubMed Mancebo A, González–Diéguez ML, Cadahía V, Varela M, Pérez R, Navascués CA, et al. Annual incidence of hepatocellular carcinoma among patients with alcoholic cirrhosis and identification of risk groups. Clin Gastroenterol Hepatol. 2013;11(1):95–101. doi:10.​1016/​j.​cgh.​2012.​09.​007.CrossRefPubMed
20.
go back to reference Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology. 2004;127(5 Suppl 1):S35–50.CrossRefPubMed Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology. 2004;127(5 Suppl 1):S35–50.CrossRefPubMed
22.
go back to reference Davila JA, Morgan RO, Richardson PA, Du XL, McGlynn KA, El-Serag HB. Use of surveillance for hepatocellular carcinoma among patients with cirrhosis in the United States. Hepatology. 2010;52(1):132–41. doi:10.1002/hep.23615.CrossRefPubMed Davila JA, Morgan RO, Richardson PA, Du XL, McGlynn KA, El-Serag HB. Use of surveillance for hepatocellular carcinoma among patients with cirrhosis in the United States. Hepatology. 2010;52(1):132–41. doi:10.​1002/​hep.​23615.CrossRefPubMed
23.
go back to reference Singal AG, Yopp A, Skinner CS, Packer M, Lee WM, Tiro JA. Utilization of hepatocellular carcinoma surveillance among American patients: a systematic review. J Gen Intern Med. 2012;27(7):861–7.CrossRefPubMedPubMedCentral Singal AG, Yopp A, Skinner CS, Packer M, Lee WM, Tiro JA. Utilization of hepatocellular carcinoma surveillance among American patients: a systematic review. J Gen Intern Med. 2012;27(7):861–7.CrossRefPubMedPubMedCentral
24.
go back to reference Edenvik P, Davidsdottir L, Oksanen A, Isaksson B, Hultcrantz R, Stål P. Application of hepatocellular carcinoma surveillance in a European setting. What can we learn from clinical practice? Liver Int. 2015;35(7):1862–71.CrossRefPubMed Edenvik P, Davidsdottir L, Oksanen A, Isaksson B, Hultcrantz R, Stål P. Application of hepatocellular carcinoma surveillance in a European setting. What can we learn from clinical practice? Liver Int. 2015;35(7):1862–71.CrossRefPubMed
25.
go back to reference Hirata A, Hirata T, Takahashi Y, Nakayama T. Surveillance rates for hepatocellular carcinoma among patients with cirrhosis, chronic hepatitis B, and chronic hepatitis C based on Japanese claims database. Hepatology Research. 2016 Hirata A, Hirata T, Takahashi Y, Nakayama T. Surveillance rates for hepatocellular carcinoma among patients with cirrhosis, chronic hepatitis B, and chronic hepatitis C based on Japanese claims database. Hepatology Research. 2016
27.
go back to reference Dalton-Fitzgerald E, Tiro J, Kandunoori P, Halm EA, Yopp A, Singal AG, et al. Practice patterns and attitudes of primary care providers and barriers to surveillance of hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol. 2015;13:791–8. e1.CrossRefPubMed Dalton-Fitzgerald E, Tiro J, Kandunoori P, Halm EA, Yopp A, Singal AG, et al. Practice patterns and attitudes of primary care providers and barriers to surveillance of hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol. 2015;13:791–8. e1.CrossRefPubMed
28.
go back to reference • Singal AG, Tiro JA, Marrero JA, McCallister K, Mejias C, Adamson B et al. Mailed outreach program increases ultrasound screening of patients with cirrhosis for hepatocellular carcinoma. Gastroenterology. 2016. A practical outreach program showing a doubling of HCC screening rates with a simple intervention • Singal AG, Tiro JA, Marrero JA, McCallister K, Mejias C, Adamson B et al. Mailed outreach program increases ultrasound screening of patients with cirrhosis for hepatocellular carcinoma. Gastroenterology. 2016. A practical outreach program showing a doubling of HCC screening rates with a simple intervention
29.
go back to reference Simmons O, Fetzer D, Yokoo T, Marrero J, Yopp A, Kono Y, et al. Predictors of adequate ultrasound quality for hepatocellular carcinoma surveillance in patients with cirrhosis. Aliment Pharmacol Ther. 2017;45(1):169–77.CrossRefPubMed Simmons O, Fetzer D, Yokoo T, Marrero J, Yopp A, Kono Y, et al. Predictors of adequate ultrasound quality for hepatocellular carcinoma surveillance in patients with cirrhosis. Aliment Pharmacol Ther. 2017;45(1):169–77.CrossRefPubMed
30.
go back to reference Yu NC, Chaudhari V, Raman SS, Lassman C, Tong MJ, Busuttil RW, et al. CT and MRI improve detection of hepatocellular carcinoma, compared with ultrasound alone, in patients with cirrhosis. Clin Gastroenterol Hepatol. 2011;9(2):161–7. doi:10.1016/j.cgh.2010.09.017.CrossRefPubMed Yu NC, Chaudhari V, Raman SS, Lassman C, Tong MJ, Busuttil RW, et al. CT and MRI improve detection of hepatocellular carcinoma, compared with ultrasound alone, in patients with cirrhosis. Clin Gastroenterol Hepatol. 2011;9(2):161–7. doi:10.​1016/​j.​cgh.​2010.​09.​017.CrossRefPubMed
31.
go back to reference Pocha C, Dieperink E, McMaken K, Knott A, Thuras P, Ho S. Surveillance for hepatocellular cancer with ultrasonography vs. computed tomography—a randomised study. Aliment Pharmacol Ther. 2013;38(3):303–12.CrossRefPubMed Pocha C, Dieperink E, McMaken K, Knott A, Thuras P, Ho S. Surveillance for hepatocellular cancer with ultrasonography vs. computed tomography—a randomised study. Aliment Pharmacol Ther. 2013;38(3):303–12.CrossRefPubMed
32.
go back to reference • Kim SY, An J, Lim Y-S, Han S, Lee J-Y, Byun JH et al. MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma. JAMA Oncology. 2016. A prospective study comparing ultrasound to MRI-based HCC surveillance • Kim SY, An J, Lim Y-S, Han S, Lee J-Y, Byun JH et al. MRI with liver-specific contrast for surveillance of patients with cirrhosis at high risk of hepatocellular carcinoma. JAMA Oncology. 2016. A prospective study comparing ultrasound to MRI-based HCC surveillance
33.
go back to reference • Marks RM, Ryan A, Heba ER, Tang A, Wolfson TJ, Gamst AC et al. Diagnostic per-patient accuracy of an abbreviated hepatobiliary phase gadoxetic acid-enhanced MRI for hepatocellular carcinoma surveillance. American Journal of Roentgenology. 2015;204(3):527–35. Proof of principle of effectiveness of an abbreviated MRI protocol for HCC surveillance • Marks RM, Ryan A, Heba ER, Tang A, Wolfson TJ, Gamst AC et al. Diagnostic per-patient accuracy of an abbreviated hepatobiliary phase gadoxetic acid-enhanced MRI for hepatocellular carcinoma surveillance. American Journal of Roentgenology. 2015;204(3):527–35. Proof of principle of effectiveness of an abbreviated MRI protocol for HCC surveillance
34.
go back to reference Besa C, Lewis S, Pandharipande PV, Chhatwal J, Kamath A, Cooper N et al. Hepatocellular carcinoma detection: diagnostic performance of a simulated abbreviated MRI protocol combining diffusion-weighted and T1-weighted imaging at the delayed phase post gadoxetic acid. Abdominal Radiology. 2016:1–12 Besa C, Lewis S, Pandharipande PV, Chhatwal J, Kamath A, Cooper N et al. Hepatocellular carcinoma detection: diagnostic performance of a simulated abbreviated MRI protocol combining diffusion-weighted and T1-weighted imaging at the delayed phase post gadoxetic acid. Abdominal Radiology. 2016:1–12
36.
go back to reference Reig M, Mariño Z, Perelló C, Iñarrairaegui M, Ribeiro A, Lens S, et al. Unexpected high rate of early tumor recurrence in patients with HCV-related HCC undergoing interferon-free therapy. J Hepatol. 2016;65(4):719–26.CrossRefPubMed Reig M, Mariño Z, Perelló C, Iñarrairaegui M, Ribeiro A, Lens S, et al. Unexpected high rate of early tumor recurrence in patients with HCV-related HCC undergoing interferon-free therapy. J Hepatol. 2016;65(4):719–26.CrossRefPubMed
37.
go back to reference Conti F, Buonfiglioli F, Scuteri A, Crespi C, Bolondi L, Caraceni P, et al. Early occurrence and recurrence of hepatocellular carcinoma in HCV-related cirrhosis treated with direct-acting antivirals. J Hepatol. 2016;65(4):727–33.CrossRefPubMed Conti F, Buonfiglioli F, Scuteri A, Crespi C, Bolondi L, Caraceni P, et al. Early occurrence and recurrence of hepatocellular carcinoma in HCV-related cirrhosis treated with direct-acting antivirals. J Hepatol. 2016;65(4):727–33.CrossRefPubMed
38.
go back to reference El‐Serag HB, Kanwal F, Richardson P, Kramer J. Risk of hepatocellular carcinoma after sustained virologic response in veterans with HCV‐infection. Hepatology. 2016 El‐Serag HB, Kanwal F, Richardson P, Kramer J. Risk of hepatocellular carcinoma after sustained virologic response in veterans with HCV‐infection. Hepatology. 2016
39.
go back to reference Baumert TF, Jühling F, Atsushi O, Hoshida Y. Hepatitis C-related hepatocellular carcinoma in the era of new generation antivirals. BMC Med. 2017 (in press). Baumert TF, Jühling F, Atsushi O, Hoshida Y. Hepatitis C-related hepatocellular carcinoma in the era of new generation antivirals. BMC Med. 2017 (in press).
40.
go back to reference Levin B, Lieberman DA, McFarland B, Smith RA, Brooks D, Andrews KS, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi‐Society Task Force on Colorectal Cancer, and the American College of Radiology*†. CA Cancer J Clin. 2008;58(3):130–60.CrossRefPubMed Levin B, Lieberman DA, McFarland B, Smith RA, Brooks D, Andrews KS, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi‐Society Task Force on Colorectal Cancer, and the American College of Radiology*†. CA Cancer J Clin. 2008;58(3):130–60.CrossRefPubMed
41.
go back to reference Tice JA, Cummings SR, Smith-Bindman R, Ichikawa L, Barlow WE, Kerlikowske K. Using clinical factors and mammographic breast density to estimate breast cancer risk: development and validation of a new predictive model. Ann Intern Med. 2008;148(5):337–47.CrossRefPubMedPubMedCentral Tice JA, Cummings SR, Smith-Bindman R, Ichikawa L, Barlow WE, Kerlikowske K. Using clinical factors and mammographic breast density to estimate breast cancer risk: development and validation of a new predictive model. Ann Intern Med. 2008;148(5):337–47.CrossRefPubMedPubMedCentral
42.
go back to reference Parmigiani G, Chen S, Iversen ES, Friebel TM, Finkelstein DM, Anton-Culver H, et al. Validity of models for predicting BRCA1 and BRCA2 mutations. Ann Intern Med. 2007;147(7):441–50.CrossRefPubMedPubMedCentral Parmigiani G, Chen S, Iversen ES, Friebel TM, Finkelstein DM, Anton-Culver H, et al. Validity of models for predicting BRCA1 and BRCA2 mutations. Ann Intern Med. 2007;147(7):441–50.CrossRefPubMedPubMedCentral
44.
go back to reference Tanabe KK, Lemoine A, Finkelstein DM, Kawasaki H, Fujii T, Chung RT, et al. Epidermal growth factor gene functional polymorphism and the risk of hepatocellular carcinoma in patients with cirrhosis. JAMA. 2008;299(1):53–60. doi:10.1001/jama.2007.65.CrossRefPubMed Tanabe KK, Lemoine A, Finkelstein DM, Kawasaki H, Fujii T, Chung RT, et al. Epidermal growth factor gene functional polymorphism and the risk of hepatocellular carcinoma in patients with cirrhosis. JAMA. 2008;299(1):53–60. doi:10.​1001/​jama.​2007.​65.CrossRefPubMed
46.
48.
go back to reference • King LY, Canasto-Chibuque C, Johnson KB, Yip S, Chen X, Kojima K, et al. A genomic and clinical prognostic index for hepatitis C-related early-stage cirrhosis that predicts clinical deterioration. Gut. 2014. doi:10.1136/gutjnl-2014-307862. Molecular risk stratification of patients with early stage cirrhosis using a gene expression molecular score.PubMedPubMedCentral • King LY, Canasto-Chibuque C, Johnson KB, Yip S, Chen X, Kojima K, et al. A genomic and clinical prognostic index for hepatitis C-related early-stage cirrhosis that predicts clinical deterioration. Gut. 2014. doi:10.​1136/​gutjnl-2014-307862. Molecular risk stratification of patients with early stage cirrhosis using a gene expression molecular score.PubMedPubMedCentral
50.
go back to reference Nakagawa S, Wei L, Song W, Higashi T, Ghoshal S, Kim RS et al. Molecular liver cancer prevention in cirrhosis by organ transcriptome analysis and lysophosphatidic acid pathway inhibition. Cancer Cell. 2016, in press. Nakagawa S, Wei L, Song W, Higashi T, Ghoshal S, Kim RS et al. Molecular liver cancer prevention in cirrhosis by organ transcriptome analysis and lysophosphatidic acid pathway inhibition. Cancer Cell. 2016, in press.
51.
go back to reference Furlan A, Marin D, Agnello F, Di Martino M, Di Marco V, Lagalla R, et al. Hepatocellular carcinoma presenting at contrast-enhanced multi-detector-row computed tomography or gadolinium-enhanced magnetic resonance Imaging as a small (≤2 cm), indeterminate nodule: growth rate and optimal interval time for imaging follow-up. J Comput Assist Tomogr. 2012;36(1):20–5.CrossRefPubMed Furlan A, Marin D, Agnello F, Di Martino M, Di Marco V, Lagalla R, et al. Hepatocellular carcinoma presenting at contrast-enhanced multi-detector-row computed tomography or gadolinium-enhanced magnetic resonance Imaging as a small (≤2 cm), indeterminate nodule: growth rate and optimal interval time for imaging follow-up. J Comput Assist Tomogr. 2012;36(1):20–5.CrossRefPubMed
52.
go back to reference Taouli B, Goh JS, Lu Y, Qayyum A, Yeh BM, Merriman RB, et al. Growth rate of hepatocellular carcinoma: evaluation with serial computed tomography or magnetic resonance imaging. J Comput Assist Tomogr. 2005;29(4):425–9.CrossRefPubMed Taouli B, Goh JS, Lu Y, Qayyum A, Yeh BM, Merriman RB, et al. Growth rate of hepatocellular carcinoma: evaluation with serial computed tomography or magnetic resonance imaging. J Comput Assist Tomogr. 2005;29(4):425–9.CrossRefPubMed
53.
go back to reference Santi V, Trevisani F, Gramenzi A, Grignaschi A, Mirici-Cappa F, Del Poggio P, et al. Semiannual surveillance is superior to annual surveillance for the detection of early hepatocellular carcinoma and patient survival. J Hepatol. 2010;53(2):291–7.CrossRefPubMed Santi V, Trevisani F, Gramenzi A, Grignaschi A, Mirici-Cappa F, Del Poggio P, et al. Semiannual surveillance is superior to annual surveillance for the detection of early hepatocellular carcinoma and patient survival. J Hepatol. 2010;53(2):291–7.CrossRefPubMed
54.
go back to reference Trinchet JC, Chaffaut C, Bourcier V, Degos F, Henrion J, Fontaine H, et al. Ultrasonographic surveillance of hepatocellular carcinoma in cirrhosis: a randomized trial comparing 3- and 6-month periodicities. Hepatology. 2011;54(6):1987–97. doi:10.1002/hep.24545.CrossRefPubMed Trinchet JC, Chaffaut C, Bourcier V, Degos F, Henrion J, Fontaine H, et al. Ultrasonographic surveillance of hepatocellular carcinoma in cirrhosis: a randomized trial comparing 3- and 6-month periodicities. Hepatology. 2011;54(6):1987–97. doi:10.​1002/​hep.​24545.CrossRefPubMed
55.
go back to reference Sarasin FP, Giostra E, Hadengue A. Cost-effectiveness of screening for detection of small hepatocellular carcinoma in western patients with Child-Pugh class A cirrhosis. Am J Med. 1996;101(4):422–34.CrossRefPubMed Sarasin FP, Giostra E, Hadengue A. Cost-effectiveness of screening for detection of small hepatocellular carcinoma in western patients with Child-Pugh class A cirrhosis. Am J Med. 1996;101(4):422–34.CrossRefPubMed
57.
go back to reference Goossens N, Singal AG, King LY, Andersson KL, Fuchs BC, Besa C et al., editors. Cost-effectiveness of a risk-stratified hepatocellular carcinoma surveillance strategy in patients with cirrhosis. HEPATOLOGY; 2016: WILEY-BLACKWELL 111 RIVER ST, HOBOKEN 07030–5774, NJ USA Goossens N, Singal AG, King LY, Andersson KL, Fuchs BC, Besa C et al., editors. Cost-effectiveness of a risk-stratified hepatocellular carcinoma surveillance strategy in patients with cirrhosis. HEPATOLOGY; 2016: WILEY-BLACKWELL 111 RIVER ST, HOBOKEN 07030–5774, NJ USA
58.
go back to reference Yoshihiroshimauchi M, Ryokokuromatsu RO, Yukiotateishi S, ONO N, Yutani S, Hiroakinagamatsu S, et al. A simultaneous monitoring of Lens culinaris agglutinin a-reactive a-fetoprotein and des-γ-carboxy prothrombin as an early diagnosis of hepatocellular carcinoma in the follow-up of cirrhotic patients. Oncol Rep. 2000;7:249–56. Yoshihiroshimauchi M, Ryokokuromatsu RO, Yukiotateishi S, ONO N, Yutani S, Hiroakinagamatsu S, et al. A simultaneous monitoring of Lens culinaris agglutinin a-reactive a-fetoprotein and des-γ-carboxy prothrombin as an early diagnosis of hepatocellular carcinoma in the follow-up of cirrhotic patients. Oncol Rep. 2000;7:249–56.
59.
go back to reference Volk ML, Hernandez JC, Su GL, Lok AS, Marrero JA. Risk factors for hepatocellular carcinoma may impair the performance of biomarkers: a comparison of AFP, DCP, and AFP-L3. Cancer Biomark. 2007;3(2):79–87.CrossRefPubMed Volk ML, Hernandez JC, Su GL, Lok AS, Marrero JA. Risk factors for hepatocellular carcinoma may impair the performance of biomarkers: a comparison of AFP, DCP, and AFP-L3. Cancer Biomark. 2007;3(2):79–87.CrossRefPubMed
60.
go back to reference Sterling RK, Jeffers L, Gordon F, Sherman M, Venook AP, Reddy KR, et al. Clinical utility of AFP-L3% measurement in North American patients with HCV-related cirrhosis. Am J Gastroenterol. 2007;102(10):2196–205.CrossRefPubMed Sterling RK, Jeffers L, Gordon F, Sherman M, Venook AP, Reddy KR, et al. Clinical utility of AFP-L3% measurement in North American patients with HCV-related cirrhosis. Am J Gastroenterol. 2007;102(10):2196–205.CrossRefPubMed
61.
go back to reference Lok AS, Sterling RK, Everhart JE, Wright EC, Hoefs JC, Di Bisceglie AM, et al. Des-γ-carboxy prothrombin and α-fetoprotein as biomarkers for the early detection of hepatocellular carcinoma. Gastroenterology. 2010;138(2):493–502.CrossRefPubMed Lok AS, Sterling RK, Everhart JE, Wright EC, Hoefs JC, Di Bisceglie AM, et al. Des-γ-carboxy prothrombin and α-fetoprotein as biomarkers for the early detection of hepatocellular carcinoma. Gastroenterology. 2010;138(2):493–502.CrossRefPubMed
62.
go back to reference Wang M, Long RE, Comunale MA, Junaidi O, Marrero J, Di Bisceglie AM, et al. Novel fucosylated biomarkers for the early detection of hepatocellular carcinoma. Cancer Epidemiol Biomark Prev. 2009;18(6):1914–21.CrossRef Wang M, Long RE, Comunale MA, Junaidi O, Marrero J, Di Bisceglie AM, et al. Novel fucosylated biomarkers for the early detection of hepatocellular carcinoma. Cancer Epidemiol Biomark Prev. 2009;18(6):1914–21.CrossRef
63.
go back to reference Marrero JA, Romano PR, Nikolaeva O, Steel L, Mehta A, Fimmel CJ, et al. GP73, a resident Golgi glycoprotein, is a novel serum marker for hepatocellular carcinoma. J Hepatol. 2005;43(6):1007–12.CrossRefPubMed Marrero JA, Romano PR, Nikolaeva O, Steel L, Mehta A, Fimmel CJ, et al. GP73, a resident Golgi glycoprotein, is a novel serum marker for hepatocellular carcinoma. J Hepatol. 2005;43(6):1007–12.CrossRefPubMed
64.
go back to reference Tian L, Wang Y, Xu D, Gui J, Jia X, Tong H, et al. Serological AFP/Golgi protein 73 could be a new diagnostic parameter of hepatic diseases. Int J Cancer. 2011;129(8):1923–31.CrossRefPubMed Tian L, Wang Y, Xu D, Gui J, Jia X, Tong H, et al. Serological AFP/Golgi protein 73 could be a new diagnostic parameter of hepatic diseases. Int J Cancer. 2011;129(8):1923–31.CrossRefPubMed
65.
go back to reference Shang S, Plymoth A, Ge S, Feng Z, Rosen HR, Sangrajrang S, et al. Identification of osteopontin as a novel marker for early hepatocellular carcinoma. Hepatology. 2012;55(2):483–90. doi:10.1002/hep.24703.CrossRefPubMed Shang S, Plymoth A, Ge S, Feng Z, Rosen HR, Sangrajrang S, et al. Identification of osteopontin as a novel marker for early hepatocellular carcinoma. Hepatology. 2012;55(2):483–90. doi:10.​1002/​hep.​24703.CrossRefPubMed
66.
go back to reference Duarte-Salles T, Misra S, Stepien M, Plymoth A, Muller D, Overvad K, et al. Circulating osteopontin and prediction of hepatocellular carcinoma development in a large European population. Cancer Prev Res (Phila). 2016;9(9):758–65. doi:10.1158/1940-6207.CAPR-15-0434.CrossRef Duarte-Salles T, Misra S, Stepien M, Plymoth A, Muller D, Overvad K, et al. Circulating osteopontin and prediction of hepatocellular carcinoma development in a large European population. Cancer Prev Res (Phila). 2016;9(9):758–65. doi:10.​1158/​1940-6207.​CAPR-15-0434.CrossRef
67.
go back to reference Hippo Y, Watanabe K, Watanabe A, Midorikawa Y, Yamamoto S, Ihara S, et al. Identification of soluble NH2-terminal fragment of glypican-3 as a serological marker for early-stage hepatocellular carcinoma. Cancer Res. 2004;64(7):2418–23.CrossRefPubMed Hippo Y, Watanabe K, Watanabe A, Midorikawa Y, Yamamoto S, Ihara S, et al. Identification of soluble NH2-terminal fragment of glypican-3 as a serological marker for early-stage hepatocellular carcinoma. Cancer Res. 2004;64(7):2418–23.CrossRefPubMed
68.
go back to reference Beneduce L, Castaldi F, Marino M, Quarta S, Ruvoletto M, Benvegnu L, et al. Squamous cell carcinoma antigen-immunoglobulin M complexes as novel biomarkers for hepatocellular carcinoma. Cancer. 2005;103(12):2558–65. doi:10.1002/cncr.21106.CrossRefPubMed Beneduce L, Castaldi F, Marino M, Quarta S, Ruvoletto M, Benvegnu L, et al. Squamous cell carcinoma antigen-immunoglobulin M complexes as novel biomarkers for hepatocellular carcinoma. Cancer. 2005;103(12):2558–65. doi:10.​1002/​cncr.​21106.CrossRefPubMed
70.
go back to reference Z-q Z, Meng H, Wang N, Liang LN, Liu LN, Lu SM, et al. Serum microRNA 143 and microRNA 215 as potential biomarkers for the diagnosis of chronic hepatitis and hepatocellular carcinoma. Diagn Pathol. 2014;9(1):1.CrossRef Z-q Z, Meng H, Wang N, Liang LN, Liu LN, Lu SM, et al. Serum microRNA 143 and microRNA 215 as potential biomarkers for the diagnosis of chronic hepatitis and hepatocellular carcinoma. Diagn Pathol. 2014;9(1):1.CrossRef
71.
go back to reference Lin X-J, Chong Y, Guo Z-W, Xie C, Yang X-J, Zhang Q, et al. A serum microRNA classifier for early detection of hepatocellular carcinoma: a multicentre, retrospective, longitudinal biomarker identification study with a nested case-control study. Lancet Oncol. 2015;16(7):804–15.CrossRefPubMed Lin X-J, Chong Y, Guo Z-W, Xie C, Yang X-J, Zhang Q, et al. A serum microRNA classifier for early detection of hepatocellular carcinoma: a multicentre, retrospective, longitudinal biomarker identification study with a nested case-control study. Lancet Oncol. 2015;16(7):804–15.CrossRefPubMed
72.
go back to reference Liu XE, Desmyter L, Gao CF, Laroy W, Dewaele S, Vanhooren V, et al. N-glycomic changes in hepatocellular carcinoma patients with liver cirrhosis induced by hepatitis B virus. Hepatology. 2007;46(5):1426–35. doi:10.1002/hep.21855.CrossRefPubMed Liu XE, Desmyter L, Gao CF, Laroy W, Dewaele S, Vanhooren V, et al. N-glycomic changes in hepatocellular carcinoma patients with liver cirrhosis induced by hepatitis B virus. Hepatology. 2007;46(5):1426–35. doi:10.​1002/​hep.​21855.CrossRefPubMed
73.
go back to reference Biselli M, Conti F, Gramenzi A, Frigerio M, Cucchetti A, Fatti G, et al. A new approach to the use of α-fetoprotein as surveillance test for hepatocellular carcinoma in patients with cirrhosis. Br J Cancer. 2015;112(1):69–76.CrossRefPubMed Biselli M, Conti F, Gramenzi A, Frigerio M, Cucchetti A, Fatti G, et al. A new approach to the use of α-fetoprotein as surveillance test for hepatocellular carcinoma in patients with cirrhosis. Br J Cancer. 2015;112(1):69–76.CrossRefPubMed
75.
go back to reference Hung Y-C, Lin C-L, Liu C-J, Hung H, Lin S-M, Lee S-D, et al. Development of risk scoring system for stratifying population for hepatocellular-carcinoma screening. Hepatology. 2015;61:1934–44. doi:10.1002/hep.27610.CrossRefPubMed Hung Y-C, Lin C-L, Liu C-J, Hung H, Lin S-M, Lee S-D, et al. Development of risk scoring system for stratifying population for hepatocellular-carcinoma screening. Hepatology. 2015;61:1934–44. doi:10.​1002/​hep.​27610.CrossRefPubMed
77.
go back to reference Velázquez RF, Rodríguez M, Navascués CA, Linares A, Pérez R, Sotorríos NG, et al. Prospective analysis of risk factors for hepatocellular carcinoma in patients with liver cirrhosis. Hepatology. 2003;37(3):520–7. doi:10.1053/jhep.2003.50093.CrossRefPubMed Velázquez RF, Rodríguez M, Navascués CA, Linares A, Pérez R, Sotorríos NG, et al. Prospective analysis of risk factors for hepatocellular carcinoma in patients with liver cirrhosis. Hepatology. 2003;37(3):520–7. doi:10.​1053/​jhep.​2003.​50093.CrossRefPubMed
78.
82.
go back to reference Yang HI, Yuen MF, Chan HLY, Han KH, Chen PJ, Kim DY, et al. Risk estimation for hepatocellular carcinoma in chronic hepatitis B (REACH-B): development and validation of a predictive score. Lancet Oncol. 2011;12(6):568–74. doi:10.1016/S1470-2045(11)70077-8.CrossRefPubMed Yang HI, Yuen MF, Chan HLY, Han KH, Chen PJ, Kim DY, et al. Risk estimation for hepatocellular carcinoma in chronic hepatitis B (REACH-B): development and validation of a predictive score. Lancet Oncol. 2011;12(6):568–74. doi:10.​1016/​S1470-2045(11)70077-8.CrossRefPubMed
83.
go back to reference Ikeda M, Fujiyama S, Tanaka M, Sata M, Ide T, Yatsuhashi H, et al. Risk factors for development of hepatocellular carcinoma in patients with chronic hepatitis C after sustained response to interferon. J Gastroenterol. 2005;40(2):148–56. doi:10.1007/s00535-004-1519-2.CrossRefPubMed Ikeda M, Fujiyama S, Tanaka M, Sata M, Ide T, Yatsuhashi H, et al. Risk factors for development of hepatocellular carcinoma in patients with chronic hepatitis C after sustained response to interferon. J Gastroenterol. 2005;40(2):148–56. doi:10.​1007/​s00535-004-1519-2.CrossRefPubMed
84.
go back to reference Chang KC, Hung CH, Lu SN, Wang JH, Lee CM, Chen CH, et al. A novel predictive score for hepatocellular carcinoma development in patients with chronic hepatitis C after sustained response to pegylated interferon and ribavirin combination therapy. J Antimicrob Chemother. 2012;67(11):2766–72. doi:10.1093/jac/dks269.CrossRefPubMed Chang KC, Hung CH, Lu SN, Wang JH, Lee CM, Chen CH, et al. A novel predictive score for hepatocellular carcinoma development in patients with chronic hepatitis C after sustained response to pegylated interferon and ribavirin combination therapy. J Antimicrob Chemother. 2012;67(11):2766–72. doi:10.​1093/​jac/​dks269.CrossRefPubMed
88.
go back to reference Shin SH, Kim SU, Park JY, Kim Do Y, Ahn SH, Han KH, et al. Liver stiffness-based model for prediction of hepatocellular carcinoma in chronic hepatitis B virus infection: comparison with histological fibrosis. Liver Int. 2015;35(3):1054–62. doi:10.1111/liv.12621.CrossRefPubMed Shin SH, Kim SU, Park JY, Kim Do Y, Ahn SH, Han KH, et al. Liver stiffness-based model for prediction of hepatocellular carcinoma in chronic hepatitis B virus infection: comparison with histological fibrosis. Liver Int. 2015;35(3):1054–62. doi:10.​1111/​liv.​12621.CrossRefPubMed
89.
go back to reference Suh B, Park S, Shin DW, Yun JM, Yang H-K, Yu SJ, et al. High liver fibrosis index FIB-4 is highly predictive of hepatocellular carcinoma in chronic hepatitis B carriers. Hepatology. 2015;61(4):1261–8. doi:10.1002/hep.27654.CrossRefPubMed Suh B, Park S, Shin DW, Yun JM, Yang H-K, Yu SJ, et al. High liver fibrosis index FIB-4 is highly predictive of hepatocellular carcinoma in chronic hepatitis B carriers. Hepatology. 2015;61(4):1261–8. doi:10.​1002/​hep.​27654.CrossRefPubMed
91.
go back to reference Ji J, Eggert T, Budhu A, Forgues M, Takai A, Dang H, et al. Hepatic stellate cell and monocyte interaction contributes to poor prognosis in hepatocellular carcinoma. Hepatology. 2015. doi:10.1002/hep.27822. Ji J, Eggert T, Budhu A, Forgues M, Takai A, Dang H, et al. Hepatic stellate cell and monocyte interaction contributes to poor prognosis in hepatocellular carcinoma. Hepatology. 2015. doi:10.​1002/​hep.​27822.
Metadata
Title
Tailored Algorithms for Hepatocellular Carcinoma Surveillance: Is One-Size-Fits-All Strategy Outdated?
Authors
Nicolas Goossens
C. Billie Bian
Yujin Hoshida
Publication date
01-03-2017
Publisher
Springer US
Published in
Current Hepatology Reports / Issue 1/2017
Electronic ISSN: 2195-9595
DOI
https://doi.org/10.1007/s11901-017-0336-z

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